Bokhari et al.,
The Journal of Animal & Plant Sciences, 22(3): 2012, Page:J.576-583
Anim. Plant Sci. 22(3):2012
ISSN: 1018-7081
INFLUENCE OF RENAL ULTRASONOGRAPHIC FINDINGS ON GFR DURING
CHRONIC UNILATERAL URETERAL OBSTRUCTION IN DOGS
S. G. Bokhari, J. Hou*, M. Iqbal**, Y. Wu* and Y. Wang*
Faculty of Veterinary Science, University of Veterinary & Animal Sciences, Lahore, 54000, Pakistan.
*
College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, 210095, P.R. China.
**
Central Veterinary Hospital, Al-Wathba, Abu Dhabi, 10829, UAE.
Corresponding Author Email: jfhou@njau.edu.cn
ABSTRACT
Renal sonographic findings can now be implicated for prediction of changes in Glomerular filtration rate, and estimation
of the degree of renal dysfunction in pets. This was successfully determined during a 20-day chronic unilateral ureteral
obstruction in experimental dogs. GFR was quantitatively measured following a single intravenous bolus of inulin. The
total clearance of the marker was calculated from the decrease in serum concentrations using a two-compartment model.
Changes in renal architecture (i.e. length, width, depth, cortex, pelvis and ureteral dilation) were simultaneously assessed
using B-mode ultrasonography. The results showed significant changes in GFR and renal architecture. Statistical analysis
revealed minimum intragroup variance in renal length, width and depth. Linear regression analysis indicated a highly
significant average correlation coefficient (r) with low standard error of estimates (SEE) and greater predictability
between GFR and left renal dimensions of length (r=0.9454, SEE= 2.64), width (r= 0.8632, SEE= 1.69), depth
(r=0.9461, SEE= 2.11), pelvis (r=0.9035, SEE= 3.91) and left ureter (r=0.9714, SEE= 2.07). The prediction error
was about 9-12%. Conclusively, ultrasonographic changes in renal dimensions, particularly renal length, width and depth
may successfully be used in dogs for prediction of changes in GFR, without the need to perform complicated laboratory
procedures in future.
Keywords: ureteral obstruction; GFR; ultrasonography; dogs.
The glomerular filtration rate (GFR) is currently
considered the best parameter for direct quantitative
assessment of overall renal function (Brown, 2003;
Laroute et al, 1999). The single-injection clearance of
Inulin is an attractive, cheap, precise and effective
alternative to the other more complicated and expensive
methods; however the set-back lies in the method being
time-consuming and hence, less commonly applied in
routine veterinary practice, making the clinician
ultimately rely upon routine laboratory indices. For
qualitative assessment of renal architecture, B-mode
ultrasonography is currently one of the most sensitive,
least-invasive diagnostic modality, providing additional
benefits of direct visualization of normal structure of
internal organs, characterization and location of lesions
and collection of biopsy samples. (DiBartola, 2005;
Hager et al, 1985; Konde et al., 1984). Recent studies
conducted in humans negate the misconception that
sonography is unable to provide information on renal
function. It has now been proved by some scientists that
renal sonography provides useful information about renal
function. Similar data in animals has not yet been
researched.
The present study was thus conducted to evaluate
the architectural and functional changes in renal tissue in
experimental models mimicking unilateral obstructive
uropathy; and thus to ascertain the best correlation and
INTRODUCTION
Urine outflow obstruction, due to calculi,
inflammatory disease, neoplasia, stricture or accidental
ureteral ligation during ovariohysterectomy, is the
common presenting complaint in face of a currently
increasing frequency of urinary tract disorders in pets
(Brown, 2003). Undiagnosed, neglected, or untreated
cases can lead to renal hydronephrosis, and hence,
progression of an acute reversible condition to a chronic
irreversible malady.
In unilateral ureteral obstruction, compensatory
renal responses mask the injury and its effect on the renal
patient during the first phase of renal damage. The animal
is not azotemic but may only have some reduced urine
concentrating ability (Klahr et al., 1988; Watson et al.,
2002a; Brown, 2003). Furthermore, as reported by Braun
and Lefebvre (2008), and Brown (2003), the large renal
functional reserve ensures maximal compensation, so that
clinical signs and routine laboratory indices generally do
not indicate severity of the renal disease, until 75% of
renal mass is destroyed. The results of this experimental
study correlated exactly well with all these findings
mentioned above. Hence, this necessitates the
implementation of additional and precise diagnostic aids
for early assessment of the degree of renal damage and
successful monitoring for follow-up patients.
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J. Anim. Plant Sci. 22(3):2012
degree of predictability of GFR values using gray-scale
sonographic changes observed in the affected kidney, for
futuristic convenience and success in monitoring
progressive renal disease in dogs.
samples were obtained at time 0 (i.e. before injection),
and at one, three, 10, 20, 40, 80 and 120 min after
injection. The samples were allowed to clot and were
centrifuged at 3000 rpm for 10-15 min; the serum thus
collected was frozen at 20 °C until analysis.
MATERIALS AND METHODS
Laboratory analysis: The concentration of Inulin was
measured with an optimized colorimetric method.
Dogs: Twenty-four healthy mongrel dogs of either sex,
aged from 6 months to 6 years and weighing 6 to 11 kg
were selected in this study. The study protocol was
approved by the Animal Ethics Committee of the Nanjing
Police Dog Research Institute of Public Security
Ministry. After acclimatization and complete health
check-up, jugular catheterization was performed using a
16 gauge indwelling catheter, for convenient blood
sampling (Bright, 2003). Just a day before the launching
of the experimental study, the left ureter was ligated in
each dog through a midline laparotomy, to create
experimental models of obstructive uropathy.
Inulin assay: The concentration of Inulin in each serum
test sample was determined by a chemical method using
anthrone reagent (Wright and Gann, 1966; Jung et al.,
1990) and spectrophotometric readings were taken at an
absorbance value of 636 nm.
The concentration profile following bolus injection
of Inulin showed a biphasic behavior pattern: the initial
rapid decrease in the plasma level was followed by a
phase of gradual decline. Such a time curve can be
described by the sum of two exponential functions (Jung
et al., 1992). For this reason, a two-compartment model
was considered to suitably fit the curve, and used to
calculate the glomerular filtration rate with the aid of the
computer software 3P97, using the formula (Sapirstein et
al., 1955):
GFR = dose
A/a + B/b
Where
GFR
= glomerular filtration rate
A
= intercept of the rapid phase
B
= intercept of the terminal phase
a
= first-order rate constant of the
Rapid phase
b
= first-order rate constant of the
terminal phase.
Test substances: For the direct quantitative assessment
of renal function, Inulin (50g equivalent to 173.7g) was
purchased from China National Medicines Corporation
Ltd., Beijing, and used as test marker.
For each kinetic study, Inulin was reconstituted
aseptically with 0.9% saline solution to obtain a final
concentration of 250mg. mL-1 (Miyamoto, K, 1998;
Laroute et al., 1999).
Real-time ultrasonographic scans of all dogs were
performed after the kinetic studies, using a small animal
ultrasound unit granted by Keen Trade Co., Wuxi, China.
Experimental design: The dogs were randomly assigned
to four groups of six animals each. In all experimental
dogs, direct measurement of renal function was carried
out to quantitate the degree of damage, using Inulin
plasma clearance assays.
For precise functional assessment of the various
stages of renal dysfunction, each kinetic study was
carried out on 0, 1, 3, 5, 7, 11, 15 and 20 days after the
left ureteral ligation. Day 0 dogs served as control (i.e.
before ureteral ligation).
Prior to the clearance studies, food was withheld
for at least 12 hours, however, the dogs were provided
free access to water before and during the procedure
(Haller et al., 1998; Laroute et al., 1999).
Ultrasonography: B-mode ultrasound assessment was
performed on the same day as the kinetic studies, in order
to assess the qualitative changes in renal tissue, during
progression of the renal dysfunction in experimental
dogs.
After appropriate patient preparation (i.e. hair
clipping from ventral abdomen, thorough cleaning of the
skin with surgical spirit, and application of acoustic gel)
(Mattoon, et al., 2002), both right and left kidneys were
scanned in standard sagittal and transverse planes
(Nyland et al., 2002; Holt, 2008), using a 5.0 MHz
convex-array curvilinear transducer. Length, width,
depth, thickness of cortex, distance of pelves of each
kidney and opening of the left ureter were recorded.
Inulin clearance: On each day of the kinetic study,
Inulin was administered, as a single intravenous injection,
at a dose rate of 100 mg/kg, via an indwelling catheter
placed in the cephalic vein of either limb (Laroute et al.,
1999). The catheter was flushed with 4 mL of saline
solution (0.9% NaCl) after the injection. The total
duration of administration of Inulin was 20 seconds.
Blood samples were obtained from the jugular vein via
the indwelling jugular catheter. For Inulin assays, blood
Statistical Analysis: The results were analyzed by
application of ANOVA for calculation of the means.
Correlations of GFR with left renal dimensions were
assessed through linear regression analysis. All statistical
analyses were performed with SAS statistical software
(SAS Institute Inc., USA).
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Bokhari et al.,
J. Anim. Plant Sci. 22(3):2012
different variables (GFR and renal length, width, depth,
pelvis, cortex and ureter) are shown in Table 2. The
relative intra-group variance expressed as CV% was least
for renal width, length and depth, respectively, as
compared to GFR (~7 vs 39%). The average co-efficient
of variation (CV%) was increasingly high for renal
cortex, pelvis and ureter (21, 41 and 53%, respectively),
suggesting higher variance.
RESULTS
Changes in Renal Function assessed through
calculated Mean GFR values: In the experimental dogs,
the GFR value decreased gradually with progression of
renal disease after ureteral ligation. Hence, from a normal
recorded mean value of 2.585± 0.225 mL. min-1. kg-1 on
Day 0, GFR showed a highly significant decrease on
Days 3, 8 and 11 (P<0.01); the least recorded mean value
of GFR was 0.754±0.063 mL. min-1. kg-1 on Day 20
(P<0.05)- Table 1.
Linear Regression Analysis and Calculation of
Correlation Coefficient between GFR and Left Renal
Dimensions: Table 3 summarizes the results of linear
regression analysis; the correlation coefficient (r) and
standard error of estimate (SEE) are shown. GFR is found
to be highly correlated with ultrasonographic changes
recorded in the left kidney, post-ligation, with a high
value of r and low SEE. The correlation coefficient (r) of
GFR with left renal length, and the standard error of
estimate (SEE), respectively, are -0.9454 and 2.64. GFR
also exhibits a high correlation with left kidney width,
depth, pelvis and ureteral opening, the values of r and
SEE respectively, being -0.8632 and 1.69 (GFR and
width), -0.9461 and 2.11 (GFR and depth), -0.9035 and
3.91 (GFR and left renal pelvis), and -0.9714 and 2.07
(GFR and left ureteral opening). Predictability was
greatest between GFR and length, depth and left ureteral
size (P<0.0001), moderately between GFR and width and
pelvis (P<0.01) and lesser between GFR and cortex
(P<0.05). The predicition error was about 9-12%. In
comparison with other variables, smaller intra-group
variabilitiy (CV%) between renal dimensions of length,
width and depth, smaller SEE and high correlation of the
variables with GFR, enhanced the overall accuracy in
predictability of GFR, through the regression equation
(Fig. 2).
Changes in Renal Architecture assessed through
Ultrasonographic findings: During the 20-day ureteral
ligation, left renal length, width and depth showed
enormous increases (Table 1). When compared with Day
0, the changes in left renal length, width and depth on
each day were highly significant (P<0.01).
Left renal pelvis, likewise, showed significant
increase in size from 7.37± 0.32 on Day 0, to 26.14±3.40
mm on Day 20 (Fig. 1C). When compared with Day 0,
the changes were significant (P<0.05 on Days 2 and 3,
and P<0.01 on Days 4, 6, 8, 10, 12, 14, 17 and 20,
respectively). Similarly, when compared with Day 0
findings, a significant decrease in left renal cortical
thickness was observed on Days 10 and 12 (P<0.05);
thereafter, the decrease in cortical thickness due to
pressure atrophy of renal tissue, was highly significant
i.e. P<0.01 on Days 14, 17 and 20, respectively (Fig.
1E).
Changes in the opening of the left ureter were
most conspicuous and significant on each day, ranging
from 1.00± 1.00 mm on Day 0 to 23.28± 2.44 mm on
Day 20 (P< 0.01) – (Table 1 and Fig. 1).
The Measured Values of GFR and Renal Dimensions
in Experimental Dogs: The average values of the
Table 1. Quantitative Changes in GFR and Left Renal Length, Width, Depth, Pelvis, Cortex and Left Ureteral
Opening During the 20-Day Experimental Period
Day
GFR
(ml/min/kg)
Left Renal
Length (mm)
Left Renal
Width (mm)
Left Renal
Depth (mm)
Left Renal
Pelvis (mm)
Left Renal
Cortex
(mm)
0
2.58±0.23
51.58±0.76
27.87±0.58
25.87±0.43
7.37±0.18
5.52±0.22
1
1.96±0.11a
59.92±0.93a
34.58±0.64a
31.75±0.55a
9.87±0.37a
5.35±0.22a
3
1.48±0.09a
61.58±0.82a
34.16±0.99a
31.87±0.49a
11.79±0.32a
5.17±0.27a
a
a
a
a
a
5
1.324±0.09
61.37±0.96
34.83±0.65
34.54±0.43
15.67±0.39
4.61±0.21a
a
a
a
a
a
8
1.32±0.09
63.25±0.85
33.08±0.60
34.21±0.49
16.25±0.43
3.82±0.23a
a
a
a
a
a
11
1.21±0.12
66.50±0.76
34.37±0.41
38.54±0.47
22.12±0.55
3.48±0.18a
a
a
a
a
a
15
1.37±0.15
68.46±1.06
35.92±0.82
39.17±0.63
24.08±0.78
4.0±0.24a
a
a
a
a
a
20
0.75±0.13
67.25±1.02
36.33±0.80
40.29±0.87
26.17±1.00
3.74±0.22a
N.B.
a: P<0.001, means highly significant,
b: P<0.01, means moderate significance;
c: P<0.05, means significant;
NS: P>0.05, means non-significant.
578
Left Upper
Ureteral
Opening
(mm)
1.17±0.08
6.62±0.29a
9.33±0.27a
13.83±0.59a
14.67±0.52a
17.12±0.49a
17.83±0.88a
23.29±0.92a
Bokhari et al.,
J. Anim. Plant Sci. 22(3):2012
(A) Sagittal Scan of Left Kidney-Day 1- length x
depth=51 x 27 mm
(B) Sagittal Scan of Left KidneyDay 8- length x
depth=51 x 32mm
(C) Sagittal Scan of Left Kidney-Day 14: Interpelves distance:18mm
(D) Transverse Scan of Left Kidney- Day 14: width x
depth= 28 x 28 mm.
(E) Sagittal Scan of Left Kidney-Day 20- cortex
thickness: 3 mm
(F) Transverse Scan of Left Kidney-Day 20: width x
depth= 34 x 37 mm .
Fig. 1 Ultrasound Scans showing Prominent Changes in Renal Architecture
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J. Anim. Plant Sci. 22(3):2012
Table 2. Average Coefficient of Variation of GFR and Renal Dimensions
Variables
GFR
Length
Width
Depth
Pelvis
Cortex
Ureter
Average Mean±S.D
1.462±0.20
62.49±1.90
33.89±0.93
34.53±1.69
16.67±2.44
4.46±0.34
12.98±2.48
Average Coefficient of Variation (CV/ %)
39.086
8.608
7.773
13.870
41.349
21.775
53.979
Table 3. Results of Linear Regression showing high Correlation of GFR with Renal Dimensions, with high
predictability
Variables (x)
n
Formula for the Calculation of
Correlation coefficient
P values
GFR (y) in relation with renal
（r）
dimensions
Length
24
y= 7.1783-0.0909x
0.0030
0.9454a
Width
24
y=7.2245-0.1697x
0.0227
0.8632b
Depth
24
y=5.1557-0.1068x
0.0018
0.9461a
Pelvis
24
y=2.6282-0.0678x
0.0075
0.9035b
Cortex
24
y=-0.3411+0.4123x
0.8029c
0.0393
Ureter
24
y=2.4719-0.0758x
0.0001
0.9714a
N.B.
a: P<0.001, means highly significant,
b: P<0.01, means moderate significance;
c: P<0.05, means significant;
NS: P>0.05, means non-significant.
SEE
SEE
%
2.638
1.697
2.108
3.910
0.717
2.073
9.21
10.32
9.71
12.25
11.62
9.17
A- Relationship between GFR and Left Renal Length
C- Relationship between GFR and Left Renal Depth
Fig. 2. Linear Regression interrelationship between
GFR and Left Renal Dimensions
DISCUSSION
The objectives of this study were aimed towards
quantitative and qualitative determination of the degree
of renal dysfunction produced as a result of experimental
unilateral ureteral obstruction; and the interrelationship
and
prediction
of
changes
in
GFR
with
ultrasonographically observed changes in the dimensions
of the affected kidney, for futuristic convenience in GFR
BB- Relationship between GFR and Left Renal Width
580
Bokhari et al.,
J. Anim. Plant Sci. 22(3):2012
calculation in clinically ill renal patients.
In clinical situations, obstructive uropathy in pets
can lead to profound hydronephrosis, which if left
untreated or undiagnosed, can cause permanent renal
damage and chronic renal failure, as a result of pressure
atrophy of the kidney tissue (Kahn et al., 2005; Vegad
and Katiyar, 1998). Although in early stages of renal
disease in dogs, the routinely-used indices do not indicate
an ongoing disease process, however, the direct
functional markers and ultrasonographic assessment
enable the clinician to detect minute changes in GFR and
renal architecture, earlier in the course of a progressive
renal disorder, thus holding importance as regards
treatment protocols and monitoring of follow-up patients.
However, since the routine calculation of GFR is a timeconsuming procedure and alternative formulae used in
human medicine for GFR calculation are not popular in
veterinary practice, hence we have predicted significant
correlation of the functional GFR changes with
morphological changes in affected renal tissues, which
can successfully be applied to routine veterinary practice
in future.
For determination of the glomerular filtration rate,
Inulin is still the accepted “gold standard” amongst all
indicator substances; toxicity for this compound is very
low (Brown, 1994), and no side effects were observed in
this study, either (Haller et al., 1998). Furthermore, the
strategy of determining the total plasma clearance of the
test marker after a single bolus injection with repeated
blood sampling over a limited period of time (Laroute et
al., 1999), proved a time-saving, precise and better
alternative to continuous infusion or urine sampling
techniques. One striking result of this study was that
Inulin concentration could successfully be determined by
application of the two-compartment model (Haller et al.,
1998; Laroute et al., 1999).
Immediately after left ureteral ligation, a highly
significant decrease in GFR was evidenced on Days 3, 5,
8 and 11 (P<0.01). With progression of time, most
experimental dogs showed a reduced renal function, as
compared to the normal dogs (P<0.05 on Days 15 and
20). In some dogs, however, there were observable
fluctuations in the GFR value with a tendency to rebound
towards improvement at various times; this could be
attributed to the early stage of renal disease (because the
experimental study lasted less than three months); early
renal disease usually does not cause loss of the whole
nephron, and hence the GFR can be observed to be close
to normal at various times, because of the hyperfiltration
of other nephrons and other compensatory mechanisms of
the contralateral kidney. This observation of GFR
returning towards a normal value, despite slight
insignificant proteinuria, was hence not surprising
(Grauer and DiBartola, 1995). However, it was
simultaneously observed that the compensatory changes
in the body occurring alongside the inflammatory process
were not consistent or supportive to repair the
hydronephrotic lesion completely. As a result, GFR value
decreased consistently (Klahr, et al., 1988), with an
overall aggravated compromising condition of the
experimental animals, towards the end of the
experimental study.
Qualitative assessment of renal dysfunction through
sonograms obtained post-ligation, revealed that longer
the duration of urinary obstruction, greater is the degree
of dilatation (and hence, pressure atrophy) of the renal
pelvis (Canpolat et al., 1996; Cartee, et al., 1980;
D’Anjou et al., 2011). After two weeks of the
experimental study, the size of the renal pelvis increased
to about 3.54 times its normal size; the increase in renal
length and width were approximately 1.3 times the
normal value, and renal depth increased to about 1.5
times the normal. After about 3 weeks post-operatively,
the left ureter showed 23 times increase in its size from
normal (Table 1); in some dogs such immense increase in
size made it a bit difficult to discriminate between the
pressure-atrophied, enlarged pelvis, from the hydroureter.
In humans, the presence of a close correlation
between kidney size and function is reported to be helpful
in the diagnosis of renal diseases (Adibi et al., 2007;
Kariyanna et al., 2004; Paleologo et al., 2007; Widjaja et
al., 2010). For our experimental study in canines, the
relationship between GFR and affected kidney
morphology investigated through simple linear regression
analysis yielded a highly significant (inverse) correlation,
low standard error of estimate and greater predictability
between GFR and left renal length, depth and ureteral
size (Table 2). Furthermore, the results in Table 2 showed
a significantly smaller coefficient of variation for renal
length, width and depth, as compared to the GFR, thus
emphasizing smaller group variability and greater
predictability. The group variability of cortex, pelvis and
ureteral size was higher than other renal parameters, and
hence we infer that these parameters may not be
considered as reliable for prediction of GFR, as renal
length, width and depth. It can however, be hypothesized
that sonographic measurements proved to be highly
specific, while GFR measurements showed high
sensitivity and lower specificity. Additionally, in contrast
to studies in humans emphasizing greater predictability of
GFR solely through renal length, we propose that
sonographic renal length, width and depth measurements
in canine patients may prove to be highly prognostic of
GFR changes in renal disease.
It can thus be concluded that despite immense
structural damage to the renal architecture, in cases of
prolonged urine outflow obstruction, the kidneys
compromise for the functional changes by compensatory
responses which minimize the total loss in GFR.
Furthermore, sonographic measurements of affected
kidneys not only prove as a non-invasive method, rather,
renal length, width and depth correlate well with GFR
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J. Anim. Plant Sci. 22(3):2012
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values in canines. Hence, they can importantly be
employed, successfully and conveniently, in routine
veterinary clinical settings in future, for precise
measurement of renal function, assessment of the degree
of renal dysfunction in affected animals, and as an
alternative to expensive, complicated and timeconsuming methods.
(Total words: 2, 715).
Acknowledgements: This study was part of a broader
research project, and was accomplished through a
collaborative international research scholarship grant for
the PhD scholar, Dr. Shehla G. Bokhari, funded by the
Government of Pakistan-Higher Education Commission
(through Chinese Scholarship Council, P.R. China);
additional funding resources include Nanjing Agricultural
University PhD Students’ Research Funds, Keen Trade
Ltd., Wuxi, China (ultrasound machine manufacturers),
and funds drawn from projects running under China
National Fund.
The author would like to thank her devoted
teachers who guided her at each step during
accomplishment of this research work, and co-authors
and fellow workers, the integrated team-work of whom
made this study successful.
Ethical Standards: The authors hereby declare that the
experiments comply with the current laws of the country
in which they were performed and International
Standards. Furthermore, animal use ethics were adopted
as permitted by the Animal Ethics Committee of the
Nanjing Police Dog Research Institute of Public Security
Ministry, P. R. China and as guided under International
legislation.
Conflict of Interest Statement: This research work was
conducted through a scholarship grant. None of the
authors of this paper has a financial or personal
relationship with other people or organizations that could
inappropriately influence or bias the content of the paper.
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